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Cited by 72Axon Guidance and Neuronal SignalingDevelopmental Biology and Gene RegulationMarine Invertebrate Physiology and Ecology

Origin and evolution of plexins, semaphorins, and Met receptor tyrosine kinases

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Junqueira Alves, Chrystian, Yotoko, Karla, Zou, Hongyan, Friedel, Roland H.·2019·Scientific Reports
DOI 10.1038/s41598-019-38512-yPMC PMC6374515
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Abstract

The transition from unicellular to multicellular organisms poses the question as to when genes that regulate cell-cell interactions emerged during evolution. The receptor and ligand pairing of plexins and semaphorins regulates cellular interactions in a wide range of developmental and physiological contexts. We surveyed here genomes of unicellular eukaryotes and of non-bilaterian and bilaterian Metazoa and performed phylogenetic analyses to gain insight into the evolution of plexin and semaphorin families. Remarkably, we detected plexins and semaphorins in unicellular choanoflagellates, indicating their evolutionary origin in a common ancestor of Choanoflagellida and Metazoa. The plexin domain structure is conserved throughout all clades; in contrast, semaphorins are structurally diverse. Choanoflagellate semaphorins are transmembrane proteins with multiple fibronectin type III domains following the N-terminal Sema domain (termed Sema-FN). Other previously not yet described semaphorin classes include semaphorins of Ctenophora with tandem immunoglobulin domains (Sema-IG) and secreted semaphorins of Echinoderamata (Sema-SP, Sema-SI). Our study also identified Met receptor tyrosine kinases (RTKs), which carry a truncated plexin extracellular domain, in several bilaterian clades, indicating evolutionary origin in a common ancestor of Bilateria. In addition, a novel type of Met-like RTK with a complete plexin extracellular domain was detected in Lophotrochozoa and Echinodermata (termed Met-LP RTK). Our findings are consistent with an ancient function of plexins and semaphorins in regulating cytoskeletal dynamics and cell adhesion that predates their role as axon guidance molecules.

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References 64 · Cited by 72

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Authors
Junqueira Alves, C., Yotoko, K., Zou, H., & Friedel, R. H.
Affiliations
  • Universidade Federal de Viçosa (BR)
  • Icahn School of Medicine at Mount Sinai (US)
Corresponding author
Friedel, Roland H.
ORCID
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2019-02-13
Volume
9
Issue
1
Pages
1970-1970
ISSN
2045-2322 (ISSN-L)
DOI
10.1038/s41598-019-38512-y
PMC
PMC6374515
OpenAlex
W2918457706
Cited by
72
References
64
Citations by year
2026: 5 · 2025: 10 · 2024: 13 · 2023: 9 · 2022: 7 · 2021: 18 · 2020: 6 · 2019: 4
FWCI
4.18
Type
journal article
Language
en
Open access
Licence
Locations
  • Scientific Reports (publishedVersion, cc-by-sa)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (publishedVersion, other-oa)
  • Americanae (AECID Library) (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • National Council for Scientific and Technological Development
  • U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (R01 NS092735)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
Keywords
plexins, semaphorins, MET receptor tyrosine kinase, choanoflagellates, bilaterian origin, Ctenophora, Echinodermata, Lophotrochozoa, axon guidance, cell adhesion, cytoskeletal dynamics, unicellular to multicellular transition
MeSH terms
Protein Domains, Amino Acid Sequence, Animals, Echinodermata, Biological Evolution, Humans, Nerve Tissue Proteins, Receptors, Cell Surface, Cell Adhesion Molecules, Proto-Oncogene Proteins c-met, Databases, Genetic, Semaphorins, Choanoflagellata

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